The impact of climate change on the distribution of rare and endangered tree Firmiana kwangsiensis using the Maxent modeling

Abstract The upsurge in anthropogenic climate change has accelerated the habitat loss and fragmentation of wild animals and plants. The rare and endangered plants are important biodiversity elements. However, the lack of comprehensive and reliable information on the spatial distribution of these organisms has hampered holistic and efficient conservation management measures. We explored the consequences of climate change on the geographical distribution of Firmiana kwangsiensis (Malvaceae), an endangered species, to provide a reference for conservation, introduction, and cultivation of this species in new ecological zones. Modeling of the potential distribution of F. kwangsiensis under the current and two future climate scenarios in maximum entropy was performed based on 30 occurrence records and 27 environmental variables of the plant. We found that precipitation‐associated and temperature‐associated variables limited the potentially suitable habitats for F. kwangsiensis. Our model predicted 259,504 km2 of F. kwangsiensis habitat based on 25 percentile thresholds. However, the high suitable habitat for F. kwangsiensis is only about 41,027 km2. F. kwangsiensis is most distributed in Guangxi's protected areas. However, the existing reserves are only 2.7% of the total suitable habitat and 4.2% of the high suitable habitat for the plant, lower than the average protection area in Guangxi (7.2%). This means the current protected areas network is insufficient, underlining the need for alternative conservation mechanisms to protect the plant habitat. Our findings will help identify additional F. kwangsiensis localities and potential habitats and inform the development and implementation of conservation, management, and cultivation practices of such rare tree species.


| INTRODUC TI ON
A comprehensive understanding of the relationship between the geographical distribution of a species and climatic factors is a critical ecological aspect for governments and environmentalists (Lawler et al., 2009;Stocker et al., 2013), because climate change strongly impacts the geographical distribution of species, affecting ecosystems and human well-being (Du et al., 2021;Klein et al., 2008;Lawler et al., 2009;Smeraldo et al., 2021;Stocker et al., 2013;Tilman & Lehman, 2001;Zhang et al., 2018). Rare and endangered plants, one of the most important biodiversity elements, play an important role in the ecosystem, healthcare, and scientific research roles and possess economic and cultural values (Klein et al., 2008;Okigbo et al., 2008).
However, the threat of climate change and anthropogenic disturbances have caused a decline in populations and extinctions in worst cases (Clavel et al., 2011;Oliver et al., 2015;Oliver & Morecroft, 2014). Therefore, evaluating the effect of climate change on the spatial distribution of rare and endangered species reveals optimal conservation and effective management practices in protecting the most endangered species Qin, Zhao, et al., 2017).
The spatial distribution of rare and endangered plants is usually limited by their inherent characteristics and influenced by human activities. For example, increasing evidence shows that the low genetic diversity may be the main reason for the poor adaptability and narrow distribution of some rare and endangered plants (Abeli et al., 2019;Kyriazis et al., 2020). Habitat fragmentation results from excessive exploitation and utilization of natural resources, which may cause the extinction of some flora and fauna (Fischer & Lindenmayer, 2007;Qiu & Fu, 2001). The spatial distribution of rare and endangered plants could also result from dispersal limitation and demographic stochasticity (Aiba et al., 2012;Clark et al., 2018;Hubbell, 2001;Legendre et al., 2009). Early research has revealed that most endemic species are spatially aggregated due to their short-ranged dispersal (Clark et al., 2018;Condit et al., 2000;Krebs, 2001). Nevertheless, few studies have distinguished the relative contributions of environmental variables in the distribution of rare and endangered plants.
Species distribution models (SDMs) can predict the geographic distribution of individual species using local data and ecological variables (Franklin & Miller, 2009). Maxent (Maximum Entropy) is one of the powerful tools for modeling endemic species with narrow habitat ranges and few available presence-only occurrence data (Ancillotto et al., 2020;Elith et al., 2006;Kong et al., 2021;Phillips et al., 2006;Segal et al., 2021;Thapa et al., 2018). Maxent has been used in numerous studies to predict the potential distribution areas of rare and endangered species. For example, ; Qin, Zhao, et al. (2017) used this model to predict the potential distributions of Thuja sutchuenensis, a rare tree species, under paleoclimate, current climate, and future climate. Saputra and Lee (2021) constructed Maxent models for current and potential future habitats for Styrax sumatrana. Kong et al. (2021) performed similar modeling for Osmanthus fragrans. Maxent modeling can also inform conservation efforts or predict future biodiversity patterns under the then climate (Algar et al., 2009;Distler et al., 2015).
Firmiana kwangsiensis (Malvaceae) is a precious tree endemic to Guangxi, South China, but it can grow in Guangdong and Yunnan provinces. This tree species can grow in moist, welldrained, or limestone soils and tolerate several soil types (Luo et al., 2011). The beautiful shape, large three-to five-lobed leaves, and orange-red flowers make it an excellent landscaping tree species. In addition, due to its superior sonic properties, the wood is utilized for the soundboards of several Chinese instruments, including Guqin and guzheng. Ancient evidence indicates the Chinese people have used gelatin from this tree and closely related species for hair conditioning or binding since the Yuan dynasty (Yen, 1956). However, F. kwangsiensis is almost extinct due to its weak natural regeneration ability, the effects of tourism, and excessive exploitation, among other reasons. The International Union for Conservation of Nature (IUCN) has listed the plant as a "critically endangered" species Qin, Zhao, et al., 2017), and it is one of the most protected wild plants by the Chinese government (Lu et al., 2021). The geographical distribution and ecological requirements of F. kwangsiensis are largely unknown. Understanding the environmental factors influencing the distribution of F. kwangsiensis can reveal the optimal conservation measures for this species.
This study aimed (a) to predict the potential ecological distribution

| Environmental variables
Temperature, rainfall, geographical barriers, and other ecological factors, such as geological formations, influence species distribution (Kaeslin et al., 2012). To determine the environmental factors that influence the distribution of F. kwangsiensis, 19 bioclimatic variables, three biophysical variables (elevation, slope, and aspect), two ground cover factors (ground cover type and vegetation coverage rate), and three human factors (human footprint, human impact, and population density) were included in our Gridded Population of the world database v4 (GPWv4; https:// sedac.ciesin.colum bia.edu/data/colle ction/ gpw-v4). The above data were converted into ".asc" files required by Maxent modeling using the ArcGIS software.
To reduce multicollinearity among the 27 environmental variables, highly correlated variables (r ≥ .80 Pearson correlation coefficient) were eliminated from further models (Graham, 2003). Finally, 12 statistical and biologically meaningful variables were used to model the geographical distribution for F. kwangsiensis (Table 1).

| Species distribution modeling
The potential habitat of F. kwangsiensis were mapped using the maximum entropy model (Maxent version 3.4.1). In the modeling, 75% of the data was used for model training, whereas 25% of the data was used for model testing (Phillips, 2006) while keeping other values as default. Jackknife analyses were performed to determine variables that significantly influence the model reliability. The model's accuracy was assessed based on the area under the receiving operator curve (AUC). The value of AUC ranges from 0 to 1. An AUC value of 0.50 indicates better performance than random, whereas a value of 1.0 indicates perfect discrimination (Swets, 1988

| Conservation assessment
The existing nature reserves (including national, provincial, and county nature reserve) data for China were downloaded from the National Specimen Information Infrastructure (http://www.nsii.org.cn). To assess the conservation status of F. kwangsiensis, we overlaid existing nature reserves with habitat suitability class and calculated the percentages of the area included in the nature reserves (Bosso et al., 2016;Cahyaningsih et al., 2021). Priority conservation areas were identified based on the visual observation of the prediction map as highly suitable habitat that does not overlap with the existing nature reserves.

| Model results
The AUC for the Maxent model for F. kwangsiensis was 0.995 (±0.004), higher than 0.5 of the random model. Precipitation in the warmest quarter (Bio18) was the most significant factor in the model, followed by precipitation in the driest quarter (BIO17), population density in 2000 (2000), annual precipitation (BIO12), temperature seasonality (BIO4), mean temperature in the wettest quarter (BIO8), the minimum temperature in the coldest month (Bio6), and the percent tree cover (PTC; Table 1). The cumulative contribution of these eight factors for F. kwangsiensis distribution was 98.3%.

| Predicted current potential distribution
The current most suitable habitats for F. kwangsiensis in southwest Guangxi, where the tree species already exist were predicted. The most suitable habitat for the tree species in the southern Yunnan province, where the tree species is known to be absent, was also predicted. Notably, the current potential distribution of F. kwangsiensis is significantly larger than the actual occurrence of the tree, including in southern Tibet, southeast Sichuan, southeast Guangdong, southwest Guizhou, Guangxi, Fujian and Taiwan Province (Figure 2).

TA B L E 2
The suitable contemporary habitat (km 2 ) for Firmiana kwangsiensis and the suitable area under two climate scenarios in the future. The total current potential habitats for the tree in China were predicted to be 259,504 km 2 , with high suitable habitats accounting for 15.81% of this ( Table 2).

| Predicted future potential distribution
Compared with the current potential habitat, the total potential habitat under the SSP126 scenario in 2021-2040 will reduce by 13.74%, equivalent to 223,844 km 2 . The high suitable habitat will reduce by 37,301 km 2 , 9.08% less than the current potential distribution ( Table 2). The high suitability habitats are in Guangdong and Taiwan provinces, while moderate suitability will increase in Sichuan Province (Figure 3). The potential suitable distribution of F. kwangsiensis will expand under the SSP126 scenario in 2041-2060, whereas the moderately suitable habitat will increase in southern Fujian and central Yunnan (Figure 3). Compared with the 2021-2040 estimates, the total suitable habitat will increase by 29.46% to 289,798 km 2 , among which high suitable habitat will be 43,193 km 2 , 15.80% more than the high suitable habitat in 2021-2040 ( Table 2).
Under the SSP585 scenario, the moderately suitable habitat for F. kwangsiensis in 2021-2040 will be in southeast Sichuan, southeast Yunnan and southern Tibet (Figure 3). The total potential habitat for the plant during this period will increase by 3.53%, whereas the high suitable habitat will decrease by 9.33% (Table 3). In the 2041-2060 period, the suitable habitat of F. kwangsiensis in south Tibet, southeast Sichuan, southwest Yunnan and Guangdong province will decrease ( Figure 3). The total potential habitat will reduce by 22.23%, and the high suitable habitat will reduce by 4.14% ( Table 2).
The current potential distribution centroid of F. kwangsiensis was predicted to be in the southeast of Baise City of Guangxi

| Assessment of conservation status
Of the 259,504 km 2 of predicted habitat, 7016 km 2 (2.70%) lie within the 65 existing protected areas in different categories and levels.
Also, 1738 km 2 of highly suitable habitat is located in 13 other protected areas, accounting for 4.24% of the predicted high suitable area (  (Poorter & Nagel, 2000). F. kwangsiensis has only been observed in the subtropical monsoon climate regions with porous brown limestone soils with frequent soil water scarcity. Soil water stress can disrupt plant metabolism and change the morphology of a plant, thus limiting the growth of a plant or even causing death (Zhang et al., 2018). Therefore, F. kwangsiensis requires prolonged high precipitation in the growing season.
The physiological toleration hypothesis suggests that the tolerance to a specific range of temperature has often been used to explains the latitudinal distribution of a species (Stocker et al., 2013).
Also, temperature-associated bioclimatic variables are key to predicting F. kwangsiensis habitat suitability (Table 1). F. kwangsiensis grows well in warm and humid areas where the temperature seasonality is ca. 5°C, and the mean temperature in the coldest month is >8°C. This temperature in accordance with the identified climatic preference for F. kwangsiensis (Luo et al., 2011). Temperature change impacts the physiological metabolism activities such as respiration, photosynthesis and water absorption, of F. kwangsiensis, influencing the distribution of this tree species. The high temperature in summer may affect the seed germination and seedling growth of F. kwangsiensis (Baskin & Baskin, 2014). The field investigation showed that F. kwangsiensis does not grow in cold regions with a mean temperature of <0°C. Therefore, we concluded that F. kwangsiensis grows best in moisture and high-temperature climate regions, attributed to its tropical adaptation.
SDM generally represents the fundamental niches of species but not the actual niches (Falk & Mellert, 2011). Numerous factors, such as interspecific competition and plant-animal interactions that influence the dimension of a niche, are not considered when predicting the potential geographical distributions of many species (Deb et al., 2017a). In a study of the metabolic rate of 14 passerine species in the northern boundary of the United States and Canada, Root (1988) found the average temperature in January in the northern boundary of the region where the Eastern Phoebe (Sayornis phoebe) grows is −4°C. Further study indicated that the winter distribution of this avian species is directly linked to food availability. According to Huang et al. (2018), sunbirds were the major pollinators of F. kwangsiensis. Considering the northern boundary of sunbirds' distribution does not go beyond 34°N (MacKinnon, 2021), our prediction of the potential distribution of F. kwangsiensis is reliable. However, certain parameters such as species' dispersal abilities, interspecific competition, and geographical obstruction that influence the distribution of F. kwangsiensis were not considered for lack of available data. As a result, future research should explore the contribution of these parameters (Elith et al., 2006).

| Predicted potential distribution of F. kwangsiensis
Increasing evidence shows that the global average temperature is increasing, partially in response to the increased emission of greenhouse gases (Muñoz et al., 2013).  Table 2).
Climate change may cause local extinction of F. kwangsiensis and related species in some areas. However, F. kwangsiensis may adapt and grow in new habitats (Deb et al., 2017a). Changes in precipitation rate, duration, and temperature may cause phenological shifts in F. kwangsiensis, directly affecting the distribution of floral and faunal that interact with F. kwangsiensis at some point of their lifecycles.
In addition, climate change will negatively affect the distribution of numerous insects, birds, and mammals that indirectly depend on this tree species (Deb et al., 2017b).

| Conservation of F. kwangsiensis
The existing F. kwangsiensis cover is only 2.70% (7016 km 2 ) of potential habitats and 4.24% (1738 km 2 ) of high potential habitats and other land-use changes will likely amplify existing constraints on plant range shifts by hampering pollination and seed dispersal (Tucker et al., 2018). This underscores the need to not only establish more natural small protected areas to maximize protection of this endangered species but also restore biotic connectivity through the recovery of animals to increase the resilience of vegetation communities under climate change (Fricke et al., 2022).
This means that most of F. kwangsiensis habitats are currently non-protected, indicating the growing effect of anthropogenic

TA B L E 3
The overlapped area (km 2 ) between the existing protected area and the potentially suitable habitat for Firmiana kwangsiensis.

F I G U R E 4
The overlapped area between high suitable habitat and the existing protected area for Firmiana kwangsiensis.
activities and climate change on the distribution of this species.
Accordingly, we suggest that F. kwangsiensis conservation should not only rely on existing nature reserves but also include small protected-area and wildlife corridors.
In this study, we explored the consequences of climate change on the geographical distribution of F. kwangsiensis, an endangered species easily recognized in the field, to provide a reference for establishing protected areas in its potential habitat. However, data on a single species is insufficient to delimit the boundaries of protected areas.
Accordingly, more similar studies, especially the potential distribution of pollinators and seed dispersers, are needed further to inform the most suitable protected areas for F. kwangsiensis. At the same time, limited resources and human resources are the major constraints of species conservation. Therefore, it is necessary to identify priority protected areas for endangered species, and carry out small-scale conservation planning for the inadequate protected areas.
The findings of this study can inform the formulation of the conservation guidelines for F. kwangsiensis. In general, there is a need to establish F. kwangsiensis protected areas and expand the existing reserves in the high-risk regions in the contest climatic change. Our analysis further identified suitable habitats for ex situ conservation of F. kwangsiensis. Furthermore, areas without a change in F. kwangsiensis distribution in the face of climate change are possible climate change refugia regions.

ACK N OWLED G M ENTS
The authors are grateful to Dr. Yingzhuo Chen and Dr. Bo Wang for their valuable suggestions and comments on the manuscript.
We also thank Wenhua Luo and Qifeng Lu from Guangxi Institute of Botany sincerely for their help in the field investigation. This

CO N FLI C T O F I NTE R E S T
The authors declare no competing interests.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.